Companion cell mediates wound-stimulated leaf-to-leaf electrical signaling
Leaf wounding triggers rapid long-range electrical signaling that initiates systemic defense responses to protect the plants from further attack. In Arabidopsis, this process largely depends on clade three ( ) genes and In the cellular context, phloem sieve elements and xylem contact cells where GLR...
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| Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2024-06, Vol.121 (24), p.e2400639121 |
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| creator | Wu, Qian Li, Yangyang Chen, Mengjiao Kong, Xiaohang |
| description | Leaf wounding triggers rapid long-range electrical signaling that initiates systemic defense responses to protect the plants from further attack. In Arabidopsis, this process largely depends on clade three
(
) genes
and
In the cellular context, phloem sieve elements and xylem contact cells where GLRs were mostly present are implicated in the signaling events. In spite of that, the spatial requirements of different leaf cell types for leaf-to-leaf signaling remain poorly investigated. In this study, we dissected cell-type-specific long-distance wound signaling mediated by GLR3s and showed that phloem companion cells are critical in shaping the functions of GLR3.3 and GLR3.6 in the signaling pathway. GLR3.3-mediated response is phloem-specific, during which, GLR3.3 has to be renewed from companion cells to allow its function in sieve elements. GLR3.6 functions dually in ectopic phloem companion cells, in addition to xylem contact cells. Furthermore, the action of GLR3.6 in phloem is independent of its paralog GLR3.3 and probably requires synthesis of GLR3.6 from xylem contact cells. Overall, our work highlights that the phloem companion cell is crucial for both GLRs in controlling leaf-to-leaf electrical signaling. |
| doi_str_mv | 10.1073/pnas.2400639121 |
| format | Article |
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(
) genes
and
In the cellular context, phloem sieve elements and xylem contact cells where GLRs were mostly present are implicated in the signaling events. In spite of that, the spatial requirements of different leaf cell types for leaf-to-leaf signaling remain poorly investigated. In this study, we dissected cell-type-specific long-distance wound signaling mediated by GLR3s and showed that phloem companion cells are critical in shaping the functions of GLR3.3 and GLR3.6 in the signaling pathway. GLR3.3-mediated response is phloem-specific, during which, GLR3.3 has to be renewed from companion cells to allow its function in sieve elements. GLR3.6 functions dually in ectopic phloem companion cells, in addition to xylem contact cells. Furthermore, the action of GLR3.6 in phloem is independent of its paralog GLR3.3 and probably requires synthesis of GLR3.6 from xylem contact cells. Overall, our work highlights that the phloem companion cell is crucial for both GLRs in controlling leaf-to-leaf electrical signaling.</description><identifier>ISSN: 0027-8424</identifier><identifier>ISSN: 1091-6490</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.2400639121</identifier><identifier>PMID: 38838018</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Arabidopsis - genetics ; Arabidopsis - metabolism ; Arabidopsis - physiology ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; Biological Sciences ; Electric contacts ; Gene Expression Regulation, Plant ; Glutamic acid receptors ; Leaves ; Phloem ; Phloem - metabolism ; Plant Leaves - metabolism ; Plant protection ; Receptors, Glutamate - metabolism ; Signal Transduction ; Wounding ; Xylem ; Xylem - metabolism</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2024-06, Vol.121 (24), p.e2400639121</ispartof><rights>Copyright National Academy of Sciences Jun 11, 2024</rights><rights>Copyright © 2024 the Author(s). Published by PNAS. 2024</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c265t-6b918f5fa8f61af15f1a09f64c8f2551f0bd99eed485ebf2dc0de9193a886bdd3</cites><orcidid>0000-0002-4521-9036</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11181143/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11181143/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38838018$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wu, Qian</creatorcontrib><creatorcontrib>Li, Yangyang</creatorcontrib><creatorcontrib>Chen, Mengjiao</creatorcontrib><creatorcontrib>Kong, Xiaohang</creatorcontrib><title>Companion cell mediates wound-stimulated leaf-to-leaf electrical signaling</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Leaf wounding triggers rapid long-range electrical signaling that initiates systemic defense responses to protect the plants from further attack. In Arabidopsis, this process largely depends on clade three
(
) genes
and
In the cellular context, phloem sieve elements and xylem contact cells where GLRs were mostly present are implicated in the signaling events. In spite of that, the spatial requirements of different leaf cell types for leaf-to-leaf signaling remain poorly investigated. In this study, we dissected cell-type-specific long-distance wound signaling mediated by GLR3s and showed that phloem companion cells are critical in shaping the functions of GLR3.3 and GLR3.6 in the signaling pathway. GLR3.3-mediated response is phloem-specific, during which, GLR3.3 has to be renewed from companion cells to allow its function in sieve elements. GLR3.6 functions dually in ectopic phloem companion cells, in addition to xylem contact cells. Furthermore, the action of GLR3.6 in phloem is independent of its paralog GLR3.3 and probably requires synthesis of GLR3.6 from xylem contact cells. Overall, our work highlights that the phloem companion cell is crucial for both GLRs in controlling leaf-to-leaf electrical signaling.</description><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis - physiology</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Biological Sciences</subject><subject>Electric contacts</subject><subject>Gene Expression Regulation, Plant</subject><subject>Glutamic acid receptors</subject><subject>Leaves</subject><subject>Phloem</subject><subject>Phloem - metabolism</subject><subject>Plant Leaves - metabolism</subject><subject>Plant protection</subject><subject>Receptors, Glutamate - metabolism</subject><subject>Signal Transduction</subject><subject>Wounding</subject><subject>Xylem</subject><subject>Xylem - metabolism</subject><issn>0027-8424</issn><issn>1091-6490</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkc1P3DAQxS0Egi1w5oYiceESmLFjr31CaEVLKyQu7dlyYnsxcuwlTlrx3zdbPkp7GmnmN0_v6RFygnCBsGSXm2TKBW0ABFNIcYcsEBTWolGwSxYAdFnLhjYH5FMpjwCguIR9csCkZBJQLsi3Ve43JoWcqs7FWPXOBjO6Uv3KU7J1GUM_xXlhq-iMr8dcb2flouvGIXQmViWsk4khrY_InjexuOPXeUh-fL75vrqt7-6_fF1d39UdFXysRatQeu6N9AKNR-7RgPKi6aSnnKOH1irlnG0kd62ntgPrFCpmpBStteyQXL3obqZ2ttu5NA4m6s0QejM862yC_veSwoNe558aESViw2aF81eFIT9Nroy6D2Ub3ySXp6IZCE6XHISY0bP_0Mc8DXPgP5RETvmymanLF6obcimD8-9uEPS2KL0tSv8tav44_RjinX9rhv0Gc_2QuQ</recordid><startdate>20240611</startdate><enddate>20240611</enddate><creator>Wu, Qian</creator><creator>Li, Yangyang</creator><creator>Chen, Mengjiao</creator><creator>Kong, Xiaohang</creator><general>National Academy of Sciences</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-4521-9036</orcidid></search><sort><creationdate>20240611</creationdate><title>Companion cell mediates wound-stimulated leaf-to-leaf electrical signaling</title><author>Wu, Qian ; Li, Yangyang ; Chen, Mengjiao ; Kong, Xiaohang</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c265t-6b918f5fa8f61af15f1a09f64c8f2551f0bd99eed485ebf2dc0de9193a886bdd3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Arabidopsis - genetics</topic><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis - physiology</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>Biological Sciences</topic><topic>Electric contacts</topic><topic>Gene Expression Regulation, Plant</topic><topic>Glutamic acid receptors</topic><topic>Leaves</topic><topic>Phloem</topic><topic>Phloem - metabolism</topic><topic>Plant Leaves - metabolism</topic><topic>Plant protection</topic><topic>Receptors, Glutamate - metabolism</topic><topic>Signal Transduction</topic><topic>Wounding</topic><topic>Xylem</topic><topic>Xylem - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wu, Qian</creatorcontrib><creatorcontrib>Li, Yangyang</creatorcontrib><creatorcontrib>Chen, Mengjiao</creatorcontrib><creatorcontrib>Kong, Xiaohang</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wu, Qian</au><au>Li, Yangyang</au><au>Chen, Mengjiao</au><au>Kong, Xiaohang</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Companion cell mediates wound-stimulated leaf-to-leaf electrical signaling</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>2024-06-11</date><risdate>2024</risdate><volume>121</volume><issue>24</issue><spage>e2400639121</spage><pages>e2400639121-</pages><issn>0027-8424</issn><issn>1091-6490</issn><eissn>1091-6490</eissn><abstract>Leaf wounding triggers rapid long-range electrical signaling that initiates systemic defense responses to protect the plants from further attack. In Arabidopsis, this process largely depends on clade three
(
) genes
and
In the cellular context, phloem sieve elements and xylem contact cells where GLRs were mostly present are implicated in the signaling events. In spite of that, the spatial requirements of different leaf cell types for leaf-to-leaf signaling remain poorly investigated. In this study, we dissected cell-type-specific long-distance wound signaling mediated by GLR3s and showed that phloem companion cells are critical in shaping the functions of GLR3.3 and GLR3.6 in the signaling pathway. GLR3.3-mediated response is phloem-specific, during which, GLR3.3 has to be renewed from companion cells to allow its function in sieve elements. GLR3.6 functions dually in ectopic phloem companion cells, in addition to xylem contact cells. Furthermore, the action of GLR3.6 in phloem is independent of its paralog GLR3.3 and probably requires synthesis of GLR3.6 from xylem contact cells. Overall, our work highlights that the phloem companion cell is crucial for both GLRs in controlling leaf-to-leaf electrical signaling.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>38838018</pmid><doi>10.1073/pnas.2400639121</doi><orcidid>https://orcid.org/0000-0002-4521-9036</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Arabidopsis - genetics Arabidopsis - metabolism Arabidopsis - physiology Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Biological Sciences Electric contacts Gene Expression Regulation, Plant Glutamic acid receptors Leaves Phloem Phloem - metabolism Plant Leaves - metabolism Plant protection Receptors, Glutamate - metabolism Signal Transduction Wounding Xylem Xylem - metabolism |
| title | Companion cell mediates wound-stimulated leaf-to-leaf electrical signaling |
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